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Ecophysiology and Phytoremediation Potential of Heavy Metal(Loid) Accumulating Plants

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Ecophysiology and Phytoremediation Potential of Heavy Metal(Loid) Accumulating Plants View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Sydney eScholarship ECOPHYSIOLOGY AND PHYTOREMEDIATION POTENTIAL OF HEAVY METAL(LOID) ACCUMULATING PLANTS ANTHONY GEORGE KACHENKO B.Hort.Sc.(Hons) A THESIS SUBMITTED IN FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY Faculty of Agriculture Food and Natural Resources The University of Sydney New South Wales Australia — MMVIII — — CERTIFICATE OF ORIGINALITY — hereby declare that the text of this thesis is my own work, and that, to the best I of my knowledge and belief, it contains no material that has been previously published or written by another person, nor any material that has been accepted as part of the requirements for any other degree or diploma in any university or other institute of higher learning, unless due acknowledgement has been made. I also declare that the intellectual content of this thesis is original and the result of my own research and to the best of my knowledge and belief, any assistance I received in the experimentation presented, and all sources of information cited have been duly acknowledged. _______________________ Anthony George Kachenko Declared at .................................... this .......................................day of ...................................................2008 i A. G. Kachenko TO MY PARENTS ii — ABSTRACT — oil contamination with heavy metal(loid)s is a major environmental problem that S requires effective and affordable remediation technologies. The utilisation of plants to remediate heavy metal(loid)s contaminated soils has attracted considerable interest as a low cost green remediation technology. The process is referred to as phytoremediation , and this versatile technology utilises plants to phytostabilise and/or phytoextract heavy metal(loid)s from contaminated soils, thereby effectively minimising their threat to ecosystem, human and animal health. Plants that can accumulate exceptionally high concentrations of heavy metal(loid)s into above-ground biomass are referred to as hyperaccumulators , and may be exploited in phytoremediation, geobotanical prospecting and/or phytomining of low-grade ore bodies. Despite the apparent tangible benefits of utilising phytoremediation techniques, a greater understanding is required to comprehend the ecophysiological aspects of species suitable for phytoremediation purposes. A screening study was instigated to assess phytoremediation potential of several fern species for soils contaminated with cadmium (Cd), chromium (Cr), copper (Cu), nickel (Ni), lead (Pb) and zinc (Zn). Hyperaccumulation was not observed in any of the studied species, and in general, species excluded heavy metal uptake by restricting their translocation into aboveground biomass. Nephrolepis cordifolia and Hypolepis muelleri were identified as possible candidates in phytostabilisation of Cu-, Pb-, Ni- or Zn-contaminated soils and Dennstaedtia davallioides appeared favourable for use in phytostabilisation of Cu- and Zn- contaminated soils. Conversely, Blechnum nudum , B. cartilagineum, Doodia aspera and Calochlaena dubia were least tolerant to most heavy metals and were classified as being least suitable for phytoremediation purposes Ensuing studies addressed the physiology of arsenic (As) hyperaccumulation in a lesser known hyperaccumulator, Pityrogramma calomelanos var. austroamericana . The phytoremediation potential of this species was compared with that of the well known As hyperaccumulator Pteris vittata . Arsenic concentration of 3,008 mg kg –1 dry weight (DW) occurred in P. calomelanos var. austroamericana fronds when exposed to 50 mg kg –1 As without visual symptoms of phytotoxicities. Conversely, P. vittata was able to hyperaccumulate 10,753 mg As kg –1 DW when exposed to 100 mg kg –1 As without the onset iii A. G. Kachenko of phytotoxicities. In P. calomelanos var. austroamericana , As was readily translocated to fronds with concentrations 75 times greater in fronds than in roots. This species has the potential for use in phytoremediation of soils with As levels up to 50 mg kg –1. Localisation and spatial distribution of As in P. calomelanos var. austroamericana pinnule and stipe tissues was investigated using micro-proton induced X-ray emission spectrometry (µ-PIXE). Freeze-drying and freeze-substitution protocols (using tetrahydrofuran [THF] as a freeze-substitution medium) were compared to ascertain their usefulness in tissue preservation. Micro-PIXE results indicated that pinnule sections prepared by freeze-drying adequately preserved the spatial elemental distribution and tissue structure of pinnule samples. In pinnules, µ-PIXE results indicated higher As concentration than in stipe tissues, with concentrations of 3,700 and 1,600 mg As kg –1 DW, respectively. In pinnules, a clear pattern of cellular localisation was not resolved whereas vascular bundles in stipe tissues contained the highest As concentration (2,000 mg As kg –1 DW). Building on these µ-PIXE results, the chemical speciation of As in P. calomelanos var. austroamericana was determined using micro-focused X-ray fluorescence (µ-XRF) spectroscopy in conjunction with micro-focused X-ray absorption near edge structure (µ-XANES) spectroscopy. The results suggested that arsenate (As V) absorbed by roots was reduced to arsenite (As III ) in roots prior to transport through vascular tissues as As V and As III . In pinnules, As III was the predominant species, presumably as aqueous-oxygen coordinated compounds. Linear least- squares combination fits of µ-XANES spectra showed As III as the predominant component in all tissues sampled. The results also revealed that sulphur containing thiolates may, in part sequester accumulated As. The final aspect of this thesis examined several ecophysiological strategies of Ni hyperaccumulation in Hybanthus floribundus subsp. floribundus , a native Australian perennial shrub species and promising candidate in phytoremediation of Ni-contaminated soils. Micro-PIXE analysis revealed that cellular structure in leaf tissues prepared by freeze- drying was adequately preserved as compared to THF freeze-substituted tissues. Elemental distribution maps of leaves showed that Ni was preferentially localised in the adaxial epidermal tissues and leaf margin, with concentration of 10,000 kg –1 DW in both regions. Nickel concentrations in stem tissues obtained by µ-PIXE analysis were lower than in the leaf tissues (1,800 mg kg –1 vs. 7,800 mg kg –1 DW, respectively), and there was no clear pattern of iv compartmentalisation across different anatomical regions. It is possible that storage of accumulated Ni in epidermal tissues may provide Ni tolerance to this species, and may further act as a deterrent against herbivory and pathogenic attack. In H. floribundus subsp. floribundus seeds, µ-PIXE analysis did not resolve a clear pattern of Ni compartmentalisation and suggests that Ni was able to move apoplastically within the seed tissues. The role of organic acids and free amino acids (low molecular weight ligands [LMW]) in Ni detoxification in H. floribundus subsp. floribundus were quantified using high performance liquid chromatography (HPLC) and ultra performance liquid chromatography (UPLC). Nickel accumulation stimulated a significant increase in citric acid concentration in leaf extracts, and based on the molar ratios of Ni to citric acid (1.3:1–1.7:1), citric acid was sufficient to account for approximately 50% of the accumulated Ni. Glutamine, alanine and aspartic acid concentrations were also stimulated in response to Ni hyperaccumulation and accounted for up to 75% of the total free amino acid concentration in leaf extracts. Together, these LMW ligands may complex with accumulated Ni and contribute to its detoxification and storage in this hyperaccumulator species. Lastly, the hypothesis that hyperaccumulation of Ni in certain plants may act as an osmoticum under water stress (drought) was tested in context of H. floribundus subsp. floribundus . A 38% decline in water potential and a 68% decline in osmotic potential occurred between water stressed and unstressed plants, however, this was not matched by an increase in accumulated Ni. The results suggested that Ni was unlikely to play a role in osmotic adjustment in this species. Drought stressed plants exhibited a low water use efficiency which might be a conservative ecophysiological strategy enabling survival of this species in competitive water-limited environments. * * * v A. G. Kachenko — ACKNOWLEDGEMENTS — “A journey of a thousand miles begins with a single step” Lao-tzu, Chinese Philosopher (604 BC –531 BC). t must be said that when I first commenced my postgraduate studies, I was somewhat I overwhelmed with the thought of several years of original research, extensive field studies, hours of laboratory analyses, conference presentations, manuscript submissions – the litany could go on for ever. However, with careful planning, sound advice and support from several remarkable people, it was possible to negotiate hurdles, maintain momentum and focus on the onerous tasks at hand. During my final year as an undergraduate student, I can clearly recall the Dean of the Faculty of Agriculture, Food and Natural Resources (FAFNR), Professor Les Copeland, encouraging students to apply for postgraduate research scholarships. In his address, he proceeded to say that from his own experience, postgraduate study was one of the best, yet challenging times in your life. To Professor Les Copeland, I would have
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